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Comparative Gene Mapping As a Tool to Understand the Evolution of Pest Crop Insect Chromosomes

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Comparative Gene Mapping As a Tool to Understand the Evolution of Pest Crop Insect Chromosomes International Journal of Molecular Sciences Article Comparative Gene Mapping as a Tool to Understand the Evolution of Pest Crop Insect Chromosomes Mauro Mandrioli ID , Giada Zambonini and Gian Carlo Manicardi * Department of Life Sciences, University of Modena and Reggio Emilia, Modena 41125, Italy; [email protected] (M.M.); [email protected] (G.Z.) * Correspondence: [email protected]; Tel.: +39-0522-52-2059 Received: 8 August 2017; Accepted: 5 September 2017; Published: 7 September 2017 Abstract: The extent of the conservation of synteny and gene order in aphids has been previously investigated only by comparing a small subset of linkage groups between the pea aphid Acyrthosiphon pisum and a few other aphid species. Here we compared the localization of eight A. pisum scaffolds (covering more than 5 Mb and 83 genes) in respect to the Drosophila melanogaster Muller elements identifying orthologous loci spanning all the four A. pisum chromosomes. Comparison of the genetic maps revealed a conserved synteny across different loci suggesting that the study of the fruit fly Muller elements could favour the identification of chromosomal markers useful for the study of chromosomal rearrangements in aphids. A. pisum is the first aphid species to have its genome sequenced and the finding that there are several chromosomal regions in synteny between Diptera and Hemiptera indicates that the genomic tools developed in A. pisum will be broadly useful not only for the study of other aphids but also for other insect species. Keywords: aphid chromosomes; Muller elements; chromosomal rearrangements; synteny 1. Introduction A large number of insect genomes have been wholly sequenced in the last decades in order to better understand their biology and, in particular for pest crop insects, to identify genes that could represent a potential target for their control in the field [1–6]. Insects are essential to maintaining agricultural ecosystems, but some of them are pests that damage >30% of agricultural, forestry, and livestock production and cause billions in economic losses annually. Currently, the genomes of at least 140 insects have been sequenced and deposited in public databases and the availability of insect genomes and transcriptomes provided valuable resources for entomological research [1–6]. Indeed, insect genomics allowed the gain of knowledge in several fields, such as functional genomics, comparative analysis of genomic contents and their organization, as well as functional analyses of critical parameters as their capacity to transmit disease agents. A better understanding of many individual genes and gene families has been obtained as well [1–6]. However, most of these projects (except Diptera) completely lacked any information about the chromosomal localization of the identified genes and, as a consequence, the involvement of chromosomal rearrangements in insect biology has been almost neglected. Data concerning the chromosomal localization of the annotated genes could be, for instance, extremely relevant to understanding the evolution of the sex chromosomes and the sex determining system, which is a topic of great interest for pest crop insects [7,8]. The genome mapping in Diptera evidenced that in Drosophila species six different chromosome arms, the so-called “Muller elements,” constitute the building blocks for all Drosophila species. The conservation of the Muller elements extends far beyond Drosophila to, at least, tephritid fruit flies, thought to have diverged from drosophilids 60–70 million years ago, favouring the understanding of Int. J. Mol. Sci. 2017, 18, 1919; doi:10.3390/ijms18091919 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2017, 18, 1919 2 of 14 the mechanisms that shaped the evolution of the dipteran karyotype [9–15]. For instance, chromosomal arms exhibit significant remnants of homology between D. melanogaster and Anopheles gambiae, despite the fact they diverged about 250 million years ago, and about 34% of their genes colocalize in “microsyntenic” clusters [10]. The genome of the aphid Acyrthosiphon pisum has been published in 2010 [16] and it favoured a better understanding of the biology of Hemiptera, a taxon consisting of a large number of pest crops species [17,18]. Few studies have been focused on the construction of genetic maps in aphids [19]. The first densest pea aphid genetic map has been developed by Hawthorne and Via [20] with the aim to study the aphid host plant specialization. They developed a linkage map of 173 dominant amplified fragment length polymorphism (AFLP) markers grouped into four linkage groups. Successively, Braendle et al. [21] developed an additional seven AFLP markers on the X chromosome. From a cytogenetic point of view, aphid chromosomes have been studied mainly in order to identify cytogenetic markers that could be useful for taxonomic identification, as well as for the analysis of karyotype evolution [22–27]. At this time, few genes have been located on chromosomes in aphids [28,29]. In order to improve our knowledge about the gene distribution on aphid chromosomes and to suggest a strategy for the identification of chromosomal markers, here we compared the localization and composition of eight scaffolds (spanning 5.3 Mb and 83 genes) identified in A. pisum in respect to the fruit fly Muller elements. This approach allowed the identification of orthologous loci spanning all the four A. pisum chromosomes. In view of the suggestion that A. pisum shows a substantial synteny (together with conserved gene order and orientation) with other Aphidinae [30,31], our approach could be useful to extend genomic information from A. pisum to other aphid species. Lastly, comparative mapping can facilitate not only the investigation of specific evolutionary questions, but also the study of synteny at genomic scales to elucidate chromosome homology, providing a framework for predicting the location of genes in other species, including insects of agricultural interest. 2. Results In order to compare the localization of genes between the A. pisum genome and the D. melanogaster Muller elements, we identified a set of 83 A. pisum genes (isolated from 8 scaffolds) with orthologues in the fruit fly genome and verified their localization (Figures1–4). In particular, in the scaffold 003383906 we identified 13 A. pisum genes with orthologues in fruit flies that mapped on Muller elements A, B, C, and D, but 8 of 13 mapped on the Muller element A (Figure1). The scaffold 003383512 presented 10 orthologous genes in A. pisum and D. melanogaster, and five of them mapped on the fruit fly Muller element B, whereas the other ones were located in elements A, C, and E (Figure1). The scaffold 003384156 contained only three orthologues and two of them mapped on Muller element E (Figure2). The scaffold 003383644 presented 12 orthologous genes and eight of them mapped on Muller element E, whereas the others mapped on D and C elements (Figure2). The scaffold 003383818 contained 13 orthologues and three of them mapped on Muller element E, whereas the other ones mapped on A, B, C, and D elements (Figure3). The scaffold 003383768 contained 12 orthologous genes between aphids and flies, and six of them mapped on Muller element E, whereas the others mapped on A, C, and D elements (Figure3). Int. J. Mol. Sci. 2017, 18, 1919 3 of 14 Int. J. Mol. Sci. 2017, 18, 1919 3 of 13 Figure 1. Gene content and reciprocal position of genes mapped in scaffold 003383906 and 003383512 inFigureAcyrthosiphon 1. Gene content pisum (green) and reciprocal and in Drosophila position of melanogaster genes mapped(brown) in scaffold Muller 003383906 elements. and 003383512 in Acyrthosiphon pisum (green) and in Drosophila melanogaster (brown) Muller elements. Int.Int. J.J. Mol.Mol. Sci. 2017, 18, 1919 44 ofof 1413 Figure 2. Gene content and reciprocal position of genes mapped in scaffold 003384156 and 003383644 in A. pisum (green) and in D. melanogaster (brown) Muller elements. Figure 2. Gene content and reciprocal position of genes mapped in scaffold 003384156 and 003383644 in A. pisum (green) and in D. melanogaster (brown) Muller elements. Int. J. Mol. Sci. 2017, 18, 1919 5 of 14 Int. J. Mol. Sci. 2017, 18, 1919 5 of 13 Figure 3. Gene content and reciprocal position of genes mapped in scaffold 003383818 and 003383768 inFigureA. pisum 3. Gene(green) content and inandD. reciprocal melanogaster position(brown) of genes Muller mapped elements. in scaffold 003383818 and 003383768 in A. pisum (green) and in D. melanogaster (brown) Muller elements. Both the scaffold 003384165 and 003384041 contained 10 orthologous genes, but 9 out of 10 genes Both the scaffold 003384165 and 003384041 contained 10 orthologous genes, but 9 out of 10 in the scaffold 003384165 mapped on Muller element B, whereas 6 out of 12 of the scaffold 003384041 genes in the scaffold 003384165 mapped on Muller element B, whereas 6 out of 12 of the scaffold have been located on element E (the other ones in Muller elements A, B, C, and D). 003384041 have been located on element E (the other ones in Muller elements A, B, C, and D). Int.Int. J.J. Mol.Mol. Sci.Sci. 2017,, 1818,, 19191919 66 ofof 1413 Figure 4. Gene content and reciprocal position of genes mapped in scaffold 003384165 and 003384041 inFigureA. pisum 4. Gene(green) content and inandD. reciprocal melanogaster position(brown) of genes Muller mapped elements. in scaffold 003384165 and 003384041 in A. pisum (green) and in D. melanogaster (brown) Muller elements. The chromosomal localization of the eight A. pisum scaffolds has been successively investigated The chromosomal localization of the eight A. pisum scaffolds has been successively investigated by FISH. As summarized in Figure5, the scaffolds 003383768 and 003383906 mapped on the opposite by FISH. As summarized in Figure 5, the scaffolds 003383768 and 003383906 mapped on the opposite telomeres of the X chromosomes, identified since they are the unique ones with a chromomycin A3 telomeres of the X chromosomes, identified since they are the unique ones with a chromomycin A3 (CMA3)- fluorescent telomere, which is a rule in aphid complements (Figure5a,c).
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